Changes in Muscle Cell Metabolism and Mechanotransduction Are Associated with Myopathic Phenotype in a Mouse Model of Collagen VI Deficiency

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  De Palma, Sara ^a,b   Leone, Roberta ^a   Grumati, Paolo ^c   Vasso, Michele ^a,b   Polishchuk, Roman ^d   Capitanio, Daniele ^a   Braghetta, Paola ^c   Bernardi, Paolo ^c   Bonaldo, Paolo ^c   Gelfi, Cecilia ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

^d INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ADENYLATE KINASE; ADENYLATE KINASE 1; CALCIUM ION; COLLAGEN TYPE 6; CREATINE KINASE; ENOLASE; ENOLASE 3; FATTY ACID SYNTHASE; FOCAL ADHESION KINASE; FRUCTOSE BISPHOSPHATE ALDOLASE; ISOCITRATE DEHYDROGENASE 1; MUSCLE PROTEIN; PARVALBUMIN; PROTEIN ROCK1; TENASCIN; TRIOSEPHOSPHATE ISOMERASE; TROPONIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL METABOLISM; CITRIC ACID CYCLE; COLLAGEN VI DEFICIENCY; CONTROLLED STUDY; DIAPHRAGM; ELECTRON MICROSCOPY; ELECTROSPRAY MASS SPECTROMETRY; ENERGY METABOLISM; ENZYMATIC ASSAY; GASTROCNEMIUS MUSCLE; GLYCOLYSIS; IMMUNOBLOTTING; LIPOTOXICITY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MECHANOTRANSDUCTION; MOUSE; MUSCLE CELL; MUSCLE INJURY; MUSCLE METABOLISM; MUSCLE RELAXATION; MUSCLE STRENGTH; MYOPATHY; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEOMICS; TIBIALIS ANTERIOR MUSCLE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CALCIUM; COLLAGEN TYPE VI; DISEASE MODELS, ANIMAL; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; MUSCLE CELLS; MUSCLE, SKELETAL; MUSCULAR DISEASES; TIBIA;

EID: 84874258544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056716     Document Type: Article

References (81)

1. Wiberg C, Heinegard D, Wenglen C, Timpl R, Morgelin M, (2002) Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures. J Biol Chem 277: 49120-49126.
2. Grounds MD, Sorokin L, White J, (2005) Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 15: 381-391.
3. Bonnemann CG, (2011) The collagen VI-related myopathies: muscle meets its matrix. Nat Rev Neurol 7: 379-390.
4. Collins J, Bonnemann CG, (2010) Congenital muscular dystrophies: toward molecular therapeutic interventions. Curr Neurol Neurosci Rep 10: 83-91.
5. Jaalouk DE, Lammerding J, (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10: 63-73.
6. Ervasti JM, (2003) Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278: 13591-13594.
7. Chandrasekharan K, Martin PT, (2010) Genetic defects in muscular dystrophy. Methods Enzymol 479: 291-322.
8. Bethlem J, Wijngaarden GK, (1976) Benign myopathy, with autosomal dominant inheritance. A report on three pedigrees. Brain 99: 91-100.
9. Demir E, Sabatelli P, Allamand V, Ferreiro A, Moghadaszadeh B, et al. (2002) Mutations in COL6A3 cause severe and mild phenotypes of Ullrich congenital muscular dystrophy. Am J Hum Genet 70: 1446-1458.
10. Lampe AK, Bushby KM, (2005) Collagen VI related muscle disorders. J Med Genet 42: 673-685.
11. Mercuri E, Yuva Y, Brown SC, Brockington M, Kinali M, et al. (2002) Collagen VI involvement in Ullrich syndrome: a clinical, genetic, and immunohistochemical study. Neurology 58: 1354-1359.
12. Merlini L, Martoni E, Grumati P, Sabatelli P, Squarzoni S, et al. (2008) Autosomal recessive myosclerosis myopathy is a collagen VI disorder. Neurology 71: 1245-1253.
13. Nonaka I, Une Y, Ishihara T, Miyoshino S, Nakashima T, et al. (1981) A clinical and histological study of Ullrich's disease (congenital atonic-sclerotic muscular dystrophy). Neuropediatrics 12: 197-208.
14. Brinas L, Richard P, Quijano-Roy S, Gartioux C, Ledeuil C, et al. (2010) Early onset collagen VI myopathies: Genetic and clinical correlations. Ann Neurol 68: 511-520.
15. Nadeau A, Kinali M, Main M, Jimenez-Mallebrera C, Aloysius A, et al. (2009) Natural history of Ullrich congenital muscular dystrophy. Neurology 73: 25-31.
16. Ullrich O, (1930) Kongenitale, atonisch-sklerotische Muskeldystrophie, ein weiterer Typus der heredodegenerativen Erkrankungen des neuromuskulären Systems Zeitschrift für die gesamte Neurologie und Psychiatrie. 126: 171-201.
17. Jobsis GJ, Boers JM, Barth PG, de Visser M, (1999) Bethlem myopathy: a slowly progressive congenital muscular dystrophy with contractures. Brain 122 (Pt 4): 649-655.
18. Haq RU, Speer MC, Chu ML, Tandan R, (1999) Respiratory muscle involvement in Bethlem myopathy. Neurology 52: 174-176.
19. Merlini L, Bernardi P, (2008) Therapy of collagen VI-related myopathies (Bethlem and Ullrich). Neurotherapeutics 5: 613-618.
20. Bonaldo P, Braghetta P, Zanetti M, Piccolo S, Volpin D, et al. (1998) Collagen VI deficiency induces early onset myopathy in the mouse: an animal model for Bethlem myopathy. Int Rev Cell Mol Biol 7: 2135-2140.
21. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, et al. (2010) Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 16: 1313-1320.
22. Irwin WA, Bergamin N, Sabatelli P, Reggiani C, Megighian A, et al. (2003) Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat Genet 35: 367-371.
23. Bernardi P, Bonaldo P, (2008) Dysfunction of mitochondria and sarcoplasmic reticulum in the pathogenesis of collagen VI muscular dystrophies. Ann N Y Acad Sci 1147: 303-311.
24. Grumati P, Coletto L, Sandri M, Bonaldo P, (2011) Autophagy induction rescues muscular dystrophy. Autophagy 7: 426-428.
25. Izu Y, Ansorge HL, Zhang G, Soslowsky LJ, Bonaldo P, et al. (2011) Dysfunctional tendon collagen fibrillogenesis in collagen VI null mice. Matrix Biol 30: 53-61.
26. Izu Y, Ezura Y, Mizoguchi F, Kawamata A, Nakamoto T, et al. (2012) Type VI collagen deficiency induces osteopenia with distortion of osteoblastic cell morphology. Tissue Cell 44: 1-6.
27. Canato M, Dal Maschio M, Sbrana F, Raiteri R, Reggiani C, et al. (2010) Mechanical and electrophysiological properties of the sarcolemma of muscle fibers in two murine models of muscle dystrophy: col6a1-/- and mdx. J Biomed Biotechnol 2010: 981945.
28. Vigano A, Vasso M, Caretti A, Bravata V, Terraneo L, et al. (2011) Protein modulation in mouse heart under acute and chronic hypoxia. Proteomics 11: 4202-4217.
29. Janssen AJ, Trijbels FJ, Sengers RC, Smeitink JA, van den Heuvel LP, et al. (2007) Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin Chem 53: 729-734.
30. Munujos P, Coll-Canti J, Gonzalez-Sastre F, Gella FJ, (1993) Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal Biochem 212: 506-509.
31. Higdon A, Landar A, Barnes S, Darley-Usmar VM (2012) The Electrophile Responsive Proteome: Integrating Proteomics and Lipidomics with Cellular Function. Antioxid Redox Signal.
32. Kansanen E, Jyrkkanen HK, Levonen AL, (2012) Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids. Free Radic Biol Med 52: 973-982.
33. Terrasa A, Guajardo M, Catala A, (1998) Lipoperoxidation of rod outer segments of bovine retina is inhibited by soluble binding proteins for fatty acids. Mol Cell Biochem 178: 181-186.
34. Rotman N, Wahli W, (2010) PPAR modulation of kinase-linked receptor signaling in physiology and disease. Physiology (Bethesda) 25: 176-185.
35. Bishop-Bailey D, Bystrom J, (2009) Emerging roles of peroxisome proliferator-activated receptor-beta/delta in inflammation. Pharmacol Ther 124: 141-150.
36. Wagner KD, Wagner N, (2010) Peroxisome proliferator-activated receptor beta/delta (PPARbeta/delta) acts as regulator of metabolism linked to multiple cellular functions. Pharmacol Ther 125: 423-435.
37. Burri L, Thoresen GH, Berge RK (2010) The Role of PPARalpha Activation in Liver and Muscle. PPAR Res 2010.
38. Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, et al. (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY) 1: 771-783.
39. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-118.
40. Wang RH, Sengupta K, Li C, Kim HS, Cao L, et al. (2008) Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice. Cancer Cell 14: 312-323.
41. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464: 121-125.
42. Hallows WC, Lee S, Denu JM, (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci U S A 103: 10230-10235.
43. Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E, (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci U S A 103: 10224-10229.
44. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, et al. (2011) Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12: 534-541.
45. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, et al. (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17: 41-52.
46. Someya S, Yu W, Hallows WC, Xu J, Vann JM, et al. (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143: 802-812.
47. Metallo CM, Gameiro PA, Bell EL, Mattaini KR, Yang J, et al. (2012) Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481: 380-384.
48. Hammarqvist F, Wernerman J, Ali R, von der Decken A, Vinnars E, (1989) Addition of glutamine to total parenteral nutrition after elective abdominal surgery spares free glutamine in muscle, counteracts the fall in muscle protein synthesis, and improves nitrogen balance. Ann Surg 209: 455-461.
49. Des Rosiers C, Di Donato L, Comte B, Laplante A, Marcoux C, et al. (1995) Isotopomer analysis of citric acid cycle and gluconeogenesis in rat liver. Reversibility of isocitrate dehydrogenase and involvement of ATP-citrate lyase in gluconeogenesis. J Biol Chem 270: 10027-10036.
50. Yoo H, Antoniewicz MR, Stephanopoulos G, Kelleher JK, (2008) Quantifying reductive carboxylation flux of glutamine to lipid in a brown adipocyte cell line. J Biol Chem 283: 20621-20627.
51. Rennie MJ, Khogali SE, Low SY, McDowell HE, Hundal HS, et al. (1996) Amino acid transport in heart and skeletal muscle and the functional consequences. Biochem Soc Trans 24: 869-873.
52. Metallo CM, Walther JL, Stephanopoulos G, (2009) Evaluation of 13C isotopic tracers for metabolic flux analysis in mammalian cells. J Biotechnol 144: 167-174.
53. Le A, Lane AN, Hamaker M, Bose S, Gouw A, et al. (2012) Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab 15: 110-121.
54. Wise DR, Ward PS, Shay JE, Cross JR, Gruber JJ, et al. (2011) Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of alpha-ketoglutarate to citrate to support cell growth and viability. Proc Natl Acad Sci U S A 108: 19611-19616.
55. Jarvinen TA, Jozsa L, Kannus P, Jarvinen TL, Hurme T, et al. (2003) Mechanical loading regulates the expression of tenascin-C in the myotendinous junction and tendon but does not induce de novo synthesis in the skeletal muscle. J Cell Sci 116: 857-866.
56. Fluck M, Mund SI, Schittny JC, Klossner S, Durieux AC, et al. (2008) Mechano-regulated tenascin-C orchestrates muscle repair. Proc Natl Acad Sci U S A 105: 13662-13667.
57. Mackey AL, Brandstetter S, Schjerling P, Bojsen-Moller J, Qvortrup K, et al. (2011) Sequenced response of extracellular matrix deadhesion and fibrotic regulators after muscle damage is involved in protection against future injury in human skeletal muscle. FASEB J 25: 1943-1959.
58. Midwood KS, Orend G, (2009) The role of tenascin-C in tissue injury and tumorigenesis. J Cell Commun Signal 3: 287-310.
59. Knoll R, (2012) Myosin binding protein C: implications for signal-transduction. J Muscle Res Cell Motil 33: 31-42.
60. Durieux AC, Desplanches D, Freyssenet D, Fluck M, (2007) Mechanotransduction in striated muscle via focal adhesion kinase. Biochem Soc Trans 35: 1312-1313.
61. Quach NL, Rando TA, (2006) Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev Biol 293: 38-52.
62. Amano M, Nakayama M, Kaibuchi K, (2010) Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 67: 545-554.
63. Grossi M, Hiou-Feige A, Tommasi Di Vignano A, Calautti E, Ostano P, et al. (2005) Negative control of keratinocyte differentiation by Rho/CRIK signaling coupled with up-regulation of KyoT1/2 (FHL1) expression. Proc Natl Acad Sci U S A 102: 11313-11318.
64. Gelfi C, Vigano A, Ripamonti M, Pontoglio A, Begum S, et al. (2006) The human muscle proteome in aging. J Proteome Res 5: 1344-1353.
65. Moriggi M, Vasso M, Fania C, Capitanio D, Bonifacio G, et al. (2010) Long term bed rest with and without vibration exercise countermeasures: effects on human muscle protein dysregulation. Proteomics 10: 3756-3774.
66. Hoffman BD, Grashoff C, Schwartz MA, (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475: 316-323.
67. Fluck M, Ziemiecki A, Billeter R, Muntener M, (2002) Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration. J Exp Biol 205: 2337-2348.
68. Deldicque L, Van Proeyen K, Francaux M, Hespel P, (2011) The unfolded protein response in human skeletal muscle is not involved in the onset of glucose tolerance impairment induced by a fat-rich diet. Eur J Appl Physiol 111: 1553-1558.
69. Maraldi NM, Sabatelli P, Columbaro M, Zamparelli A, Manzoli FA, et al. (2009) Collagen VI myopathies: from the animal model to the clinical trial. Adv Enzyme Regul 49: 197-211.
70. Guo W, Giancotti FG, (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 5: 816-826.
71. Huang X, Yang N, Fiore VF, Barker TH, Sun Y, et al. (2012) Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am J Respir Cell Mol Biol 47: 340-348.
72. Gizak A, Majkowski M, Dus D, Dzugaj A, (2004) Calcium inhibits muscle FBPase and affects its intracellular localization in cardiomyocytes. FEBS Lett 576: 445-448.
73. Keller A, Demeurie J, Merkulova T, Geraud G, Cywiner-Golenzer C, et al. (2000) Fibre-type distribution and subcellular localisation of alpha and beta enolase in mouse striated muscle. Biol Cell 92: 527-535.
74. Mamczur P, Rakus D, Gizak A, Dus D, Dzugaj A, (2005) The effect of calcium ions on subcellular localization of aldolase-FBPase complex in skeletal muscle. FEBS Lett 579: 1607-1612.
75. Kadler KE, Hill A, Canty-Laird EG, (2008) Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20: 495-501.
76. Murphy-Ullrich JE, (2001) The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J Clin Invest 107: 785-790.
77. Schwaller B, Meyer M, Schiffmann S, (2002) 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1: 241-258.
78. Yanez M, Gil-Longo J, Campos-Toimil M, (2012) Calcium binding proteins. Adv Exp Med Biol 740: 461-482.
79. Bloch RJ, Gonzalez-Serratos H, (2003) Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31: 73-78.
80. Chopard A, Arrighi N, Carnino A, Marini JF, (2005) Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long-term bedrest with or without exercise. FASEB J 19: 1722-1724.
81. Kannus P, Jozsa L, Jarvinen TA, Jarvinen TL, Kvist M, et al. (1998) Location and distribution of non-collagenous matrix proteins in musculoskeletal tissues of rat. Histochem J 30: 799-810.